Humans track extended objects even when there are no foveal targets to guide eye position. We recently studied the contribution of the superior colliculus (SC) to this behavior. When primates tracked the invisible center of an object defined by two peripheral bars, SC activity was dominated by neurons in the SC's retinotopic map representing the center's location. Inactivation of these neurons caused constant eye position offsets, with no other motor deficits. Such offsets indicate a biased estimate of object location, but it is not clear how they emerge or why they are constant. We developed a data-driven model of SC activity during our task. By measuring the responses of 117 neurons having a range of preferred eccentricities, we estimated the spatial extent of the activity representing object location. We then simulated the effects of inactivation by scaling the estimated activity profile with a ‘suppression’ function, describing the spatial extent of the inactivation. This function was obtained by measuring visually-guided saccade latencies in each experiment: after inactivation, latencies increased for some locations but not others, providing an estimate of which SC neurons were affected. According to our model, inactivation caused an imbalance of activity across the two SC's, even though the object and gaze were aligned. This imbalance explains the emergence of an offset and its direction, but not its constancy. Such constancy was achieved through visual feedback of object location. For each simulated inactivation experiment, there existed an offset for which the retinotopic object location gave rise to a balanced activity profile across the two SC's, eliminating any further need to deviate gaze. These results explain why a constant eye position offset occurs after SC inactivation, and they support the conclusion that the SC contains a distributed representation of behaviorally-relevant locations, distinct from its representation of saccade motor commands.